Aberrant cerebral network topology and mild cognitive impairment in early Parkinson's disease

Human Brain Mapping

Volumn 36, Issue 8, 2015, Pages 2980-2995

  Pereira, Joana B ^a   Aarsland, Dag ^a,b   Ginestet, Cedric E ^c   Lebedev, Alexander V ^b   Wahlund, Lars Olof ^a   Simmons, Andrew ^c,d   Volpe, Giovanni ^e   Westman, Eric ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b STAVANGER UNIVERSITY HOSPITAL   (Norway)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d King s College London   (United Kingdom)

^e BILKENT UNIVERSITY   (Turkey)

Author keywords

characteristic path length; global efficiency; graph theory; hubs; structural co variance networks

Indexed keywords

ADULT; AGED; AMYGDALA; ARTICLE; BRAIN SIZE; CAUDATE NUCLEUS; CHARACTERISTIC PATH LENGTH; CONTROLLED STUDY; CORTICAL THICKNESS (BRAIN); FEMALE; GLOBAL EFFICIENCY; GRAY MATTER; HIPPOCAMPUS; HUMAN; INFORMATION PROCESSING; LENGTH; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MILD COGNITIVE IMPAIRMENT; MOTOR DYSFUNCTION; NERVE CELL NETWORK; NERVOUS SYSTEM PARAMETERS; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; NUCLEUS ACCUMBENS; PARKINSON DISEASE; PRIORITY JOURNAL; PUTAMEN; REDUCTION; THALAMUS; WHITE MATTER; BRAIN; BRAIN MAPPING; COMPLICATION; DISEASE COURSE; NEUROPSYCHOLOGICAL TEST; PATHOLOGY; PATHOPHYSIOLOGY;

BRAIN; BRAIN MAPPING; DISEASE PROGRESSION; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MILD COGNITIVE IMPAIRMENT; NEUROPSYCHOLOGICAL TESTS; PARKINSON DISEASE;

EID: 84946192687     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22822     Document Type: Article

References (88)

1. Achard S, Bullmore E (2007): Efficiency and cost of economical brain functional networks. PLoS Comput Biol 3:e17.
2. Agosta F, Canu E, Stefanova E, Sarro L, Tomic A, Spica V, Comi G, Kostić VS, Filippi M (2013): Mild cognitive impairment in parkinson's disease is associated with a distributed pattern of brain white matter damage. Hum Brain Mapp 35:1921–1929.
3. Alexander-Bloch A, Giedd JN, Bullmore E (2013a): Imaging structural co-variance between human brain regions. Nat Rev Neurosci 14:322–336.
4. Alexander-Bloch A, Raznahan A, Bullmore E, Giedd J (2013b): The convergence of maturational change and structural covariance in human cortical networks. J Neurosci 33:2889–2899.
5. Alves G, Lange J, Blennow K, Zetterberg H, Andreasson U, Førland MG, Tysnes O-B, Larsen JP, Pedersen KF (2014): CSF aβ42 predicts early-onset dementia in parkinson disease. Neurology 82:1784–1790.
6. Angot E, Steiner JA, Hansen C, Li JY, Brundin P (2010): Are synucleinopathies prion-like disorders? Lancet Neurol 9:1128–38. 12
7. Baggio H-C, Sala-Llonch R, Segura B, Marti M-J, Valldeoriola F, Compta Y, Tolosa E, Junqué C (2014): Functional brain networks and cognitive deficits in Parkinson's disease. Hum Brain Mapp 35:4620--4634.
8. Bassett DS, Bullmore E (2006): Small-world brain networks. Neuroscientist 12:512–523.
9. Bassett DS, Bullmore E, Verchinski BA, Mattay VS, Weinberger DR, Meyer-Lindenberg A (2008): Hierarchical organization of human cortical networks in health and schizophrenia. J Neurosci 28:9239–9248.
10. Bernhardt BC, Chen Z, He Y, Evans AC, Bernasconi N (2011): Graph-theoretical analysis reveals disrupted small-world organization of cortical thickness correlation networks in temporal lobe epilepsy. Cereb Cortex 21:2147–2157.
11. Bohbot VD, Lerch J, Thorndycraft B, Iaria G, Zijdenbos AP (2007): Gray matter differences correlate with spontaneous strategies in a human virtual navigation task. J Neurosci 27:10078–10083.
12. Braak H, Del Tredici K (2005): Poor and protracted myelination as a contributory factor to neurodegenerative disorders. Neurobiol Aging 25:19–23.
13. Braak H, Sandmann-Keil D, Gai WP, Braak E (1999): Extensive axonal lewy neurites in parkinson's disease: A novel pathological feature revealed by α-synuclein immunocytochemistry. Neurosci Lett 265:67–69.
14. Bullmore E, Sporns O (2009): Complex brain networks: Graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10:186–198.
15. Chen ZJ, He Y, Rosa-Neto P, Germann J, Evans AC (2008): Revealing modular architecture of human brain structural networks by using cortical thickness from MRI. Cereb Cortex 18:2374–2381.
16. Clauset A, Newman MEJ, Moore C (2004): Finding community structure in very large networks. Phys Rev E 70:066111.
17. Compta Y, Parkkinen L, O'Sullivan SS, Vandrovcova J, Holton JL, Collins C, Lashley T, Kallis C, Williams DR, de Silva R, Lees AJ, Revesz T (2011): Lewy- and Alzheimer-type pathologies in parkinson's disease dementia: Which is more important? Brain 134:1493–1505.
18. Cools R, Miyakawa A, Sheridan M, D'Esposito M (2010): Enhanced frontal function in parkinson's disease. Brain 133:225–233.
19. Cronin-Golomb A (2010): Parkinson's disease as a disconnection syndrome. Neuropsychol Rev 20:191–208.
20. Dale AM, Fischl B, Sereno MI (1999): Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9:179–194.
21. de Haan W, van der Flier WM, Koene T, Smits LL, Scheltens P, Stam CJ (2012): Disrupted modular brain dynamics reflect cognitive dysfunction in alzheimer's disease. Neuroimage 59:3085–3093.
22. Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ. (2006): An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 31:968–980.
23. Destrieux C, Fischl B, Dale A, Halgren E (2010): Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. Neuroimage 53:1–15.
24. Dijkstra EW (1959): A note on two problems in connexion with graphs. Num Mat 1:269–271.
25. Duvernoy HM, Cabanis EA, Vannson JL (1991): The Human Brain: Surface, Three-Dimensional Sectional Anatomy and MRI. Wien: Springer-Verlag.
26. Fahn S, Elton RL (1987): The UPDRS Development Committee. Unified Parkinson's disease rating scale. In: Fahn S, Marsden CD, Calne D, Goldstein M, editors. Recent Developments in Parkinson's disease. Florham Park, NJ: Macmillan Health Care Information. pp 153–163.
27. Filippi M, van den Heuvel MP, Fornito A, He Y, Pol HEH, Agosta F, Comi G, Rocca MA (2013): Assessment of system dysfunction in the brain through MRI-based connectomics. Lancet Neurol 12:1189--1199.
28. Fischl B, Dale AM (2000): Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 97:11050–11055.
29. Fischl B, Sereno MI, Dale AM (1999): Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage 9:195–207.
30. Fischl B, Liu A, Dale AM (2001): Automated manifold surgery: Constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Trans Med Imaging 20:70–80.
31. Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM (2002): Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron 33:341–355.
32. Fischl B, van der Kouwe A, Destrieux C, Halgren E, Segonne F, Salat DH, Busa E, Seidman LJ, Goldstein J, Kennedy D, Caviness V, Makris N, Rosen B, Dale AM (2004): Automatically parcellating the human cerebral cortex. Cereb Cortex 14:11–22.
33. Frost B, Diamond MI (2010): Prion-like mechanisms in neurodegenerative diseases. Nat Rev Neurosci 11:155–159.
34. Genovese CR, Lazar NA, Nichols T (2002): Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15:870–878.
35. Goetz CG, Fahn S, Martinez-Martin P, Poewe W, Sampaio C, Stebbins GT, Stern MB, Tilley BC, Dodel R, Dubois B, Holloway R, Jankovic J, Kulisevsky J, Lang AE, Lees A, Leurgans S, LeWitt PA, Nyenhuis D, Olanow CW, Rascol O, Schrag A, Teresi JA, Van Hilten JJ, LaPelle N (2007): Movement disorder Society-sponsored revision of the unified parkinson's disease rating scale (MDS-UPDRS): Process, format, and clinimetric testing plan. Mov Disord 22:41–47.
36. Gong G, He Y, Chen ZJ, Evans AC (2012): Convergence and divergence of thickness correlations with diffusion connections across the human cerebral cortex. Neuroimage 59:1239–1248.
37. Göttlich M, Münte TF, Heldmann M, Kasten M, Hagenah J, Krämer UM (2013): Altered resting state brain networks in parkinson's disease. PloS One 8:e77336.
38. Hattori T, Orimo S, Aoki S, Ito K, Abe O, Amano A, Sato R, Sakai K, Mizusawa H (2012): Cognitive status correlates with white matter alteration in parkinson's disease. Hum Brain Mapp 33:727–739.
39. He Y, Chen ZJ, Evans AC (2007): Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. Cereb Cortex 17:2407–2419.
40. He Y, Chen Z, Evans A (2008): Structural insights into aberrant topological patterns of large-scale cortical networks in alzheimer's disease. J Neurosci 28:4756–4766.
41. He Y, Dagher A, Chen Z, Charil A, Zijdenbos A, Worsley K, Evans A (2009a): Impaired small-world efficiency in structural cortical networks in multiple sclerosis associated with white matter lesion load. Brain 132:3366–3379.
42. He Y, Wang J, Wang L, Chen ZJ, Yan C, Yang H, Tang H, Zhu C, Gong Q, Zang Y, Evans AC (2009b): Uncovering intrinsic modular organization of spontaneous brain activity in humans. PloS One 4:e5226.
43. Helmich RC, Derikx LC, Bakker M, Scheeringa R, Bloem BR, Toni I (2010): Spatial remapping of cortico-striatal connectivity in parkinson's disease. Cereb Cortex 20:1175–1186.
44. Hoehn MH, Yahr MD (1967): Parkinsonism: Onset, progression, and mortality. Neurology 17:427–442.
45. Hosseini SM, Black JM, Soriano T, Bugescu N, Martinez R, Raman MM, Kesler SR, Hoeft F (2013): Topological properties of large-scale structural brain networks in children with familial risk for reading difficulties. Neuroimage 71:260–274.
46. Kehagia AA, Barker RA, Robbins TW (2010): Neuropsychological and clinical heterogeneity of cognitive impairment and dementia in patients with parkinson's disease. Lancet Neurol 9:1200–1213.
47. Kwak Y, Peltier S, Bohnen N, Müller M, Dayalu P, Seidler RD (2010): Altered resting state cortico-striatal connectivity in mild to moderate stage parkinson's disease. Front Syst Neurosci 4:143.
48. Lerch JP, Worsley K, Shaw WP, Greenstein DK, Lenroot RK, Giedd J, Evans AC (2006): Mapping anatomical correlations across cerebral cortex (MACACC) using cortical thickness from MRI. Neuroimage 31:993–1003.
49. Litvan I, Goldman JG, Troster AI, Schmand BA, Weintraub D, Petersen RC, Mollenhauer B, Adler CH, Marder K, Williams-Gray CH, Aarsland D, Kulisevsky J, Rodriguez-Oroz MC, Burn DJ, Barker RA, Emre M (2012): Diagnostic criteria for mild cognitive impairment in parkinson's disease: Movement disorder society task force guidelines. Mov Disord 27:349–356.
50. Luce RD, Perry AD (1949): A method of matrix analysis of group structure. Psychometrika 14:95–116.
51. Melzer TR, Watts R, MacAskill MR, Pitcher TL, Livingston L, Keenan RJ, Dalrymple-Alford JC, Anderson TJ (2013): White matter microstructure deteriorates across cognitive stages in parkinson disease. Neurology 80:1841–1849.
52. Mesulam MM (1998): From sensation to cognition. Brain 121:1013–1052.
53. Meunier D, Lambiotte R, Fornito A, Ersche KD, Bullmore ET (2009): Hierarchical modularity in human brain functional networks. Front Neuroinform 3:37.
54. Olde Dubbelink KT, Hillebrand A, Stoffers D, Deijen JB, Twisk JW, Stam CJ, Berendse HW (2014): Disrupted brain network topology in parkinson's disease: A longitudinal magnetoencephalography study. Brain 137:197–207.
55. Palop JJ, Mucke L (2010): Amyloid-β–induced neuronal dysfunction in alzheimer's disease: From synapses toward neural networks. Nat Neurosci 13:812–818.
56. Parkinson progression marker initiative (2011): The parkinson progression marker initiative (PPMI). Prog Neurobiol 95:629–635.
57. Pereira JB, Ibarretxe-Bilbao N, Marti M-J, Compta Y, Junqué C, Bargallo N Tolosa E (2012): Assessment of cortical degeneration in patients with parkinson's disease by voxel-based morphometry, cortical folding, and cortical thickness. Hum Brain Mapp 33:2521–2534.
58. Pereira JB, Svenningsson P, Weintraub D, Brønnick K, Lebedev A, Westman E, Aarsland D (2014): Initial cognitive decline is associated with cortical thinning in early parkinson's disease. Neurology 82:2017–2025.
59. Reijmer YD, Leemans A, Caeyenberghs K, Heringa SM, Koek HL, Biessels GJ (2013): Disruption of cerebral networks and cognitive impairment in alzheimer disease. Neurology 80:1370–1377.
60. Rektorova I, Biundo R, Marecek R, Weis L, Aarsland D, Antonini A (2014): Grey matter changes in cognitively impaired parkinson's disease patients. PloS One 9:e85595.
61. Rubinov M, Sporns O (2010): Complex network measures of brain connectivity: Uses and interpretations. Neuroimage 52:1059–1069.
62. Rubinov M, Sporns O (2011): Weight-conserving characterization of complex functional brain networks. Neuroimage 56:2068–2079.
63. Saito Y, Kawashima A, Ruberu NN, Fujiwara H, Koyama S, Sawabe M, Arai T, Nagura H, Yamanouchi H, Hasegawa M, Iwatsubo T, Murayama S (2003): Accumulation of phosphorylated alpha-synuclein in aging human brain. J Neuropathol Exp Neurol 62:644–654.
64. Seeley WW, Crawford RK, Zhou J, Miller BL, Greicius MD (2009): Neurodegenerative diseases target large-scale human brain networks. Neuron 62:42–52.
65. Segonne F, Dale AM, Busa E, Glessner M, Salat D, Hahn HK, Fischl B (2004): A hybrid approach to the skull stripping problem in MRI. Neuroimage 22:1060–1075.
66. Segonne F, Pacheco J, Fischl B (2007): Geometrically accurate topology-correction of cortical surfaces using nonseparating loops. IEEE Trans Med Imaging 26:518–529.
67. Siderowf A, Xie SX, Hurtig H, Weintraub D, Duda J, Chen-Plotkin A, Shaw LM, Deerlin VV, Trojanowski JQ, Clark C (2010): CSF amyloid β 1-42 predicts cognitive decline in parkinson disease. Neurology 75:1055–1061.
68. Sheikh JI, Yesavage JA (1986): Geriatric Depression Scale (GDS): Recent evidence and development of a shorter version. In: Brink TL, editor. Clinical Gerontology: A Guide to Assessment and Intervention. New York: The Haworth Press.pp 165–173.
69. Simmons A, Westman E, Muehlboeck S, Mecocci P, Vellas B, Tsolaki M, Kłoszewska I, Wahlund L-O, Soininen H, Lovestone S, Evans A, Spenger C (2011): The AddNeuroMed framework for multi-center MRI assessment of alzheimer's disease: Experience from the first 24 months. Int J Geriatr Psychiatry 26:75–82.
70. Singh MK, Kesler SR, Hadi Hosseini SM, Kelley RG, Amatya D, Hamilton JP, Chen MC, Gotlib IH (2013): Anomalous gray matter structural networks in major depressive disorder. Biol Psychiatry 74:777–785.
71. Skidmore F, Korenkevych D, Liu Y, He G, Bullmore E, Pardalos PM (2011): Connectivity brain networks based on wavelet correlation analysis in parkinson fMRI data. Neurosci Lett 499:47–51.
72. Sled JG, Zijdenbos AP, Evans AC (1998): A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17:87–97.
73. Sporns O, Honey CJ, Kötter R (2007): Identification and classification of hubs in brain networks. PloS One 2:e1049.
74. Svenningsson P, Westman E, Ballard C, Aarsland D (2012): Cognitive impairment in patients with parkinson's disease: Diagnosis, biomarkers, and treatment. Lancet Neurol 11:697–707.
75. Teicher MH, Anderson CM, Ohashi K, Polcari A (2013): Childhood maltreatment: Altered network centrality of cingulate, precuneus, temporal pole and insula. Biol Psychiatry 76:297–305.
76. van den Heuvel MP, Sporns O (2013): Network hubs in the human brain. Trends Cogn Sci 17:683–696.
77. van den Heuvel MP, Stam CJ, Kahn RS, Hulshoff Pol HE (2009): Efficiency of functional brain networks and intellectual performance. J Neurosci 29:7619–7624.
78. van Eimeren T, Monchi O, Ballanger B, Strafella AP (2009): Dysfunction of the default mode network in parkinson disease: A functional magnetic resonance imaging study. Arch Neurol 66:877–883.
79. Wang J, Zuo X, Dai Z, Xia M, Zhao Z, Zhao X, Jia J, Han Y, He Y (2013): Disrupted functional brain connectome in individuals at risk for alzheimer's disease. Biol Psychiatry 73:472–481.
80. Watts DJ, Strogatz SH (1998): Collective dynamics of ‘small-world’ networks. Nature 393:440–442.
81. Weintraub D, Dietz N, Duda JE, Wolk DA, Doshi J, Xie SX, Davatzikos C, Clark CM, Siderowf A (2012): Alzheimer's disease pattern of brain atrophy predicts cognitive decline in parkinson's disease. Brain 135:170–180.
82. Wen W, Zhu W, He Y, Kochan NA, Reppermund S, Slavin MJ, Brodaty H, Crawford J, Xia A, Sachdev P (2011): Discrete neuroanatomical networks are associated with specific cognitive abilities in old age. J Neurosci 31:1204–1212.
83. Westman E, Aguilar C, Muehlboeck JS, Simmons A (2013): Regional magnetic resonance imaging measures for multivariate analysis in alzheimer's disease and mild cognitive impairment. Brain Topogr 26:9–23.
84. Wu T, Chan P, Hallett M (2010): Effective connectivity of neural networks in automatic movements in parkinson's disease. Neuroimage 49:2581–2587.
85. Wu K, Taki Y, Sato K, Kinomura S, Goto R, Okada K, Kawashima R, He Y, Evans AC, Fukuda H (2012): Age-related changes in topological organization of structural brain networks in healthy individuals. Hum Brain Mapp 33:552–568.
86. Xia M, Wang J, He Y (2013): BrainNet viewer: A network visualization tool for human brain connectomics. PLoS One 8:e68910.
87. Yao Z, Zhang Y, Lin L, Zhou Y, Xu C Jiang T, Alzheimer's Disease Neuroimaging Initiative (2010): Abnormal cortical networks in mild cognitive impairment and alzheimer's disease. PLoS Comput Biol 6:e1001006.
88. Zhu W, Wen W, He Y, Xia A, Anstey KJ, Sachdev P (2012): Changing topological patterns in normal aging using large-scale structural networks. Neurobiol Aging 33:899–913.